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JOURNAL of NEMATOLOGY Description of Heterodera

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JOURNAL of NEMATOLOGY Description of Heterodera JOURNAL OF NEMATOLOGY Article | DOI: 10.21307/jofnem-2020-097 e2020-97 | Vol. 52 Description of Heterodera microulae sp. n. (Nematoda: Heteroderinae) from China a new cyst nematode in the Goettingiana group Wenhao Li1, Huixia Li1,*, Chunhui Ni1, Deliang Peng2, Yonggang Liu3, Ning Luo1 and Abstract 1 Xuefen Xu A new cyst-forming nematode, Heterodera microulae sp. n., was 1College of Plant Protection, Gansu isolated from the roots and rhizosphere soil of Microula sikkimensis Agricultural University/Biocontrol in China. Morphologically, the new species is characterized by Engineering Laboratory of Crop lemon-shaped body with an extruded neck and obtuse vulval cone. Diseases and Pests of Gansu The vulval cone of the new species appeared to be ambifenestrate Province, Lanzhou, 730070, without bullae and a weak underbridge. The second-stage juveniles Gansu Province, China. have a longer body length with four lateral lines, strong stylets with rounded and flat stylet knobs, tail with a comparatively longer hyaline 2 State Key Laboratory for Biology area, and a sharp terminus. The phylogenetic analyses based on of Plant Diseases and Insect ITS-rDNA, D2-D3 of 28S rDNA, and COI sequences revealed that the Pests, Institute of Plant Protection, new species formed a separate clade from other Heterodera species Chinese Academy of Agricultural in Goettingiana group, which further support the unique status of Sciences, Beijing, 100193, China. H. microulae sp. n. Therefore, it is described herein as a new species 3Institute of Plant Protection, Gansu of genus Heterodera; additionally, the present study provided the first Academy of Agricultural Sciences, record of Goettingiana group in Gansu Province, China. Lanzhou, 730070, Gansu Province, China. Keywords *E-mail: [email protected] Goettingiana group, Heterodera, Morphology, New species, Phylogeny, Taxonomy. This paper was edited by Thomas Powers. Received for publication July 5, 2020. Cyst-forming nematodes are the economical pests of Due to overlapping morphological characters cultivated crops and known to be reported from all the and phenotypic plasticity, it is difficult to distinguish continents (Jones et al., 2013). The genus Heterodera closely related Heterodera species; therefore, was erected by Schmidt (1871) and currently contains sequence-based diagnosis is gaining more reliability about 80 species (Subbotin et al., 2010). Literature for precise and accurate identification of cyst- studies have indicated the presence of 14 Heterodera forming nematodes (Peng et al., 2003). The internal species from China mainland, including H. avenae transcribed spacer region of the ribosomal DNA (Chen et al., 1991), H. glycines (Liu et al., 1994), (ITS-rDNA), the D2 and D3 expansion fragments of H. sinensis (Chen and Zheng, 1994), H. filipjevi (Li the 28S ribosomal DNA genes (D2-D3 of 28S-rDNA), et al., 2010), H. koreana (Wang et al., 2012; Wang et al., and mitochondrial DNA (COI gene) units are good 2012b), H. elachista (Ding et al., 2012), H. ripae (Wang candidate genes for molecular taxonomic and et al., 2012a; Wang et al., 2012b), H. hainanensis phylogenetic studies (Subbotin et al., 2001; Subbotin (Zhuo et al., 2013), H. fengi (Wang et al., 2013), et al., 2006; Madani et al., 2004; Vovlas et al., 2017). H. guangdongensis (Zhuo et al., 2014), H. zeae Based on morphomolecular characterizations, (Wu et al., 2017), H. sojae (Zhen et al., 2018), Handoo and Subbotin (2018) divided Heterodera into H. schachtii, and H. vallicola (Peng et al., 2020). nine distinct groups such as Afenestrata, Avenae, © 2020 Authors. This is an Open Access article licensed under the Creative 1 Commons CC BY 4.0 license, https://creativecommons.org/licenses/by/4.0/ Heterodera microulae sp. n. from China: Li et al. Bifenestra, Cardiolata, Cyperi, Goettingiana, Humuli, The 28S D2-D3 region was amplified with the D2A Sacchari, and Schachtii group. Sequence analysis of (5′-ACAAGTACCGTGAGGGAAAGTTG-3′) and D3B these groups is significant to study the phylogenetic (5′-TCGGAAGGAACCAGCTACTA-3′) (De Ley et al., relationship and identifying the Heterodera species. 2005; Ye et al., 2007). Finally, the partial COI gene During 2018 and 2019, a population of cyst was amplified using primers Het-coxiF (5′-TAGTT nematode was collected from the rhizosphere of GATCGTAATTTTAATGG-3′) and Het-coxiR (5′-CCT Microula sikkimensis in Tianzhu county of Gansu AAAACATAATGAAAATGWGC-3′) (Subbotin, 2015). Province, China. Considering the economic value PCR conditions were as described by Ye et al. (2007), of the cyst nematode, morphomolecular studies De Ley et al. (2005), and Subbotin (2015). PCR pro- were performed; the preliminary studies indicated ducts were separated on 1% agarose gels and that the population belongs to Goettingiana group visualized by staining with ethidium bromide. PCR of Heterodera. The species characters were then products of sufficiently high quality were purified for compared with all the related species and concluded cloning and sequencing by Tsingke Biotech Co. Ltd., that this population possess unique characters Xi’an, China. The PCR products were purified by the and it is described herein as Heterodera microulae Tiangen Gel Extraction Kit (Tiangen Biotech Co. Ltd., sp. n. Beijing, China), cloned into pMD18-T vectors and transformed into DH5α -competent cells, and then Materials and methods sequenced by Tsingke Biotech Co. Ltd (Xi’an, China). Isolation and morphological observation Sequence alignment and phylogenetic of nematodes analysis The nematodes were extracted from root and soil The newly obtained sequences for each gene (ITS- samples of Microula sikkimensis in Tianzhu county, rDNA, D2-D3 region of 28S-rDNA, and COI gene) Gansu Province, China. Cysts and white females were compared with known sequences of Heterodera were collected using sieving-decanting method, while using BLASTn homology search program. Outgroup second-stage juveniles (J2s) were recovered from taxa for phylogenetic analyses were selected based hatched eggs and kept in water suspension until on the previously published studies (Subbotin et al., further use (Hooper, 1970; Golden, 1990). Males were 2001; Maafi et al., 2003; Mundo-Ocampo et al., not found. For morphometric studies, second-stage 2008; Kang et al., 2016; Madani et al., 2018; Vovlas juveniles were killed by gentle heating, fixed in TAF et al., 2017). The selected sequences were aligned solution (formalin: triethanolamine: water = 7:2:91), and by MAFFT (Kazutaka and Standley, 2013) with default processed to ethanol-glycerin dehydration according parameters and edited using Gblock (Castresana, to Seinhorst (1959) as modified by De Grisse (1969) 2000). Phylogenetic analyses were based on Bayesian and mounted on permanent slides. Vulval cones inference (BI) using MrBayes 3.1.2 (Huelsenbeck and were mostly mounted in glycerin jelly. Measurements Ronquist, 2001). The GTR + I + G model was selected were made on mounted specimens using a Nikon as the best-fit model of DNA evolution for both 28S Eclipse E100 Microscope (Nikon, Tokyo, Japan). D2-D3, ITS, and COI regions using MrModeltest Light micrographs and illustrations were produced version 2.3 (Nylander, 2004), according to the Akaike using a Zeiss Axio Scope A1 microscope (Zeiss, information criterion (AIC). BI analysis for each gene Jena, Germany) equipped with an AxioCam 105 was initiated with a random starting tree and run color camera and Nikon YS 100 with a drawing tube with four Markov chains for 1,000,000 generations. (Nikon, Tokyo, Japan), respectively. The Markov chains were sampled at intervals of 100 generations and the burn-in value was 25%. Two runs Molecular analyses were performed for each analysis. After discarding burn-in samples, the remaining samples were used DNA samples were prepared according to Maria to generate a 50% majority-rule consensus tree. et al. (2018). Three sets of primers (synthesized by Posterior probabilities (PP) were given on appropriate Tsingke Biotech Co. Ltd., Xi’an, China) were used clades. The phylogenetic consensus trees were in the PCR analyses to amplify sequences of the visualized using FigTree v.1.4.3 software (http://tree. ITS, D2-D3 expansion segments of 28S, and COI bio.ed.ac.uk/software/figtree/) (Rambaut, 2016). The gene. The ITS region was amplified with TW81 species in Goettingiana group and their localities, (5′-GTTTCCGTAGGTGAACCTGC-3′) and AB28 (5′-AT hosts, and GenBank accession numbers used in this ATGCTTAAGTTCAGCGGGT-3′) (Maafi et al., 2003). study were presented in Table S1. 2 JOURNAL OF NEMATOLOGY Results brown; remnants of the subcrystalline layer were rarely present. The egg sac was usually absent (Figs. 1G, Systematics 3B, C). The vulval cone was ambifenestrate-like waning crescent moon and separated by a well-developed Heterodera microulae sp. n. (Figures 1–4; Measure- vulval bridge. The anus area was distinct, bullae were ment Table 1) absent (Figs. 1F, 3D, E). The vulval slit was longer than fenestral width (39.00 vs 37.75 µm); the underbridge Description was weak and often lost during cone preparation. Cyst Female It is lemon-shaped with an obtuse vulval cone, neck extruding, and cuticle thick with an irregular zig-zag The female was lemon-shaped, pearl white, or pale pattern. The color was white to pale to medium yellow in color. It was rarely rounded with a protruding Figure 1: Line drawing of H. microulae sp. n. A: Anterior region of second-stage juvenile; B: Head of second-stage juvenile; C: Stylet of second-stage juvenile; D: Tail of second-stage juvenile; E: Cyst; F: Fenestration in vulval cone. 3 Heterodera microulae sp. n. from China: Li et al. Figure 2: Light micrographs of H. microulae sp. n. A: females attached on M. sikkimensis; B: yellow and white females; C: Anterior region of female; D: Vulval region of female (scale bar: A = 2 mm; B = 1 mm; C, D = 20 µm). neck and vulva, the subcrystalline layer was present, was weak, the stylet was strong, and basal knobs and the egg sac absent (Figs. 2A, B, 3A). There was were rounded and anteriorly flattened. The excretory a labial region with two annuli.
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